Restricted accessResearch articleFirst published online 2017-4
Visual motion processing in migraine: Enhanced motion after-effects are related to display contrast,visual symptoms,visual triggers and attack frequency
Visual after-effects are illusions that occur after prolonged viewing of visual displays. The motion after-effect (MAE), for example, is an illusory impression of motion after viewing moving displays: subsequently, stationary displays appear to drift in the opposite direction. After-effects have been used extensively in basic vision research and in clinical settings, and are enhanced in migraine.
Objective
The objective of this article is to assess associations between (1) MAE duration and visual symptoms experienced during/between migraine/headache attacks, and (2) visual stimuli reported as migraine/headache triggers.
Methods
The MAE was elicited after viewing motion for 45 seconds. MAE duration was tested for three test contrast displays (high, medium, low). Participants also completed a headache questionnaire that included migraine/headache triggers.
Results
For each test contrast, the MAE was prolonged in migraine. MAE duration was associated with photophobia; visual triggers (flicker, striped patterns); and migraine or headache frequency.
Conclusions
Group differences on various visual tasks have been attributed to abnormal cortical processing in migraine, such as hyperexcitability, heightened responsiveness and/or a lack of intra-cortical inhibition. The results are not consistent with hyperexcitability simply from a general lack of inhibition. Alternative multi-stage models are discussed and suggestions for further research are recommended, including visual tests in clinical assessments/clinical trials.
DebneyLMVisual stimuli as migraine trigger factors. In: RoseFC (ed). Progress in migraine research, 2, London: Pitman Books Ltd, 1984.
2.
HayKMMortimerMJBarkerDC. 1044 women with migraine: The effect of environmental stimuli. Headache1994; 34: 166–168.
3.
HarleDEEvansBJ. The optometric correlates of migraine. Ophthalmic Physiol Opt2004; 24: 369–383.
4.
HarleDEShepherdAJEvansBJ. Visual stimuli are common triggers of migraine and are associated with pattern glare. Headache2006; 46: 1431–1440.
5.
ShepherdAJ. Visual stimuli, light and lighting are common triggers of migraine and headache. J Light Visual Environ2010; 34: 40–46.
6.
PeatfieldRCGawalMJRoseFC. Asymmetry of the aura and pain in migraine. J Neurol Neurosurg Psychiatry1981; 44: 846–848.
7.
RasmussenBKOlesenJ. Migraine with aura and migraine without aura: An epidemiological study. Cephalalgia1992; 12: 221–228.
8.
ShepherdAJModels of cortical function in migraine: Can psychophysical studies distinguish between them? A review of the evidence for interictal cortical hyper- and hypo-excitability. In: ClarkeLB (ed). Migraine disorders research trends. Chapter VI, New York: Nova Science Publishers Inc., 2007, pp. 145–164.
9.
McKendrickAMBadcockDR. Motion processing deficits in migraine. Cephalalgia2004; 24: 363–372.
10.
AntalATemmeJNitscheMA. Altered motion perception in migraineurs: Evidence for interictal cortical hyperexcitability. Cephalalgia2005; 25: 788–794.
11.
ShepherdAJBeaumontHMHineTJ. Motion processing deficits in migraine are related to contrast sensitivity. Cephalalgia2012; 32: 554–570.
12.
TibberMSKellyMGJansariA. An inability to exclude visual noise in migraine. Invest Ophthalmol Vis Sci2014; 55: 2539–2546.
13.
ShepherdAJ. Increased visual after-effects following pattern adaptation in migraine: A lack of intracortical excitation?Brain2001; 124: 2310–2318.
14.
ShepherdAJ. Local and global motion after-effects are both enhanced in migraine, and the underlying mechanisms differ across cortical areas. Brain2006; 129: 1833–1843.
15.
WadeNJ. A selective history of the study of visual motion aftereffects. Perception1994; 23: 1111–1134.
16.
VerstratenFAFredericksenREvan WezelRJ. Recovery from adaptation for dynamic and static motion aftereffects: Evidence for two mechanisms. Vision Res1996; 36: 421–424.
17.
HubelDHWieselTN. Receptive fields of single neurones in the cat’s striate cortex. J Physiol1959; 148: 574–591.
18.
HubelDHWieselTN. Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol1962; 160: 106–154.
19.
SteinhoffBJFreudenthalerNPaulusW. The influence of established and new antiepileptic drugs on visual perception. 1. A placebo-controlled, double-blind, single-dose study in healthy volunteers. Epilepsy Res1997; 29: 35–47.
20.
SteinhoffBJFreudenthalerNPaulusW. The influence of established and new antiepileptic drugs on visual perception. 2. A controlled study in patients with epilepsy under long-term antiepileptic medication. Epilepsy Res1997; 29: 49–58.
21.
CalvertJEHarrisJPPhillipsonOT. Tilt after-effect reveals early visual processing deficits in Parkinson’s disease and in chronic schizophrenic patients on depot neuroleptic. Psychopathology1991; 24: 375–380.
22.
HarrisJ. The duration of the movement after-effect as an index of psychiatric illness. Perception1994; 23: 1145–1153.
23.
Singh P and Shepherd AJ. Enhanced motion after-effects in migraine are related to contrast sensitivity: Implications for models of differences in precortical/cortical function. Invest Ophthalmol Vis Sci 2016; 57(3): 1228–1234.
24.
WohlgemuthA. On the after-effect of seen movement. Br J Psychol1911; 1(Suppl): 1–117.
25.
BarlowHBHillRM. Evidence for a physiological explanation for the waterfall phenomenon and figural after-effects. Nature1963; 200: 1345–1347.
26.
AnstisSVerstratenFAJMatherG. The motion after-effect. Trends Cogn Sci1998; 2: 111–117.
27.
van WezelRJBrittenKH. Motion adaptation in area MT. J Neurophysiol2002; 88: 3469–3476.
28.
van WezelRJBrittenKH. Multiple uses of visual motion. The case for stability in sensory cortex. Neuroscience2002; 111: 739–759.
MatherGVerstratenFAnstisSM. The motion aftereffect: A modern perspective, Cambridge, MA: MIT Press, 1998.
31.
KeckMJPalellaTDPantleA. Motion aftereffect as a function of the contrast of sinusoidal gratings. Vision Res1976; 16: 187–191.
32.
MarcusDASosoMJ. Migraine and stripe-induced visual discomfort. Arch Neurol1989; 46: 1129–1132.
33.
Khalil NM. Investigations of visual function in migraine using visual evoked potentials and visual psychophysical tests. PhD Thesis, University of London, UK, 1991.
34.
ShepherdAJ. Visual contrast processing in migraine. Cephalalgia2000; 20: 865–880.
35.
MullenersWMChronicleEPPalmerJE. Suppression of perception in migraine – evidence for reduced inhibition in the visual cortex. Neurology2001; 56: 178–183.
36.
ShepherdAJHineTJBeaumontHM. Colour and spatial frequency are related to visual pattern sensitivity in migraine. Headache2013; 53: 1087–1103.
37.
KaranovicOThabetMWilsonHR. Detection and discrimination of flicker contrast in migraine. Cephalalgia2011; 31: 723–736.
38.
Headache Classification Subcommittee of the International Headache Society. The International Classification of Headache Disorders: 2nd edition. Cephalalgia2004; 24(Suppl. 1): 24–36.
39.
PelliDG. The Video Toolbox software for visual psychophysics: Transforming numbers into movies. Spat Vis1994; 10: 437–442.
40.
HukACReesDHeegerDJ. Neuronal basis of the motion aftereffect reconsidered. Neuron2001; 32: 161–172.
41.
ChronicleEPMullenersW. Visual system dysfunction in migraine: A review of clinical and psychophysical findings. Cephalalgia1996; 16: 525–535.
42.
PalmerJEChronicleEPRolanP. Cortical hyperexcitability is cortical under-inhibition: Evidence from a novel functional test of migraine patients. Cephalalgia2000; 20: 525–532.
43.
VidyasagarTR. Pattern adaptation in cat visual-cortex is a cooperative phenomenon. Neuroscience1990; 36: 175–179.
44.
McLeanJPalmerLA. Contrast adaptation and excitatory amino acid receptors in cat striate cortex. Vis Neurosci1996; 13: 1069–1087.
45.
MaffeiLFiorentiniABistiS. Neural correlate of perceptual adaptation to gratings. Science1973; 182: 1036–1038.
46.
NishidaSAshidaHSatoT. Contrast dependencies of two types of motion aftereffect. Vis Res1997; 37: 553–563.
47.
TibberMSShepherdAJ. Transient tritanopia in migraine: Evidence for a large-field retinal abnormality in blue-yellow opponent pathways. Invest Ophthalmol Vis Sci2006; 47: 5125–5131.
48.
AmbrosiniAde NoordhoutAMSandorP. Electrophysiological studies in migraine: A comprehensive review of their interest and limitations. Cephalalgia2003; 23: 13–31.
49.
KroppPGerberWD. Prediction of migraine attacks using a slow cortical potential, the contingent negative variation. Neurosci Lett1998; 257: 73–76.
50.
EversSQuibeldeyFGrotemeyerKH. Dynamic changes of cognitive habituation and serotonin metabolism during the migraine interval. Cephalalgia1999; 19: 485–491.
51.
JuditASandorPSSchoenenJ. Habituation of visual and intensity dependence of auditory evoked cortical potentials tends to normalize just before and during the migraine attack. Cephalalgia2000; 20: 714–719.
52.
SiniatchkinMGerberWDKroppP. How the brain anticipates an attack: A study of neurophysiological periodicity in migraine. Funct Neurol1999; 14: 69–77.
53.
SiniatchkinMKroppPGerberWD. Migraine in childhood – are periodically occurring migraine attacks related to dynamic changes of cortical information processing?Neurosci Lett2000; 279: 1–4.
54.
SiniatchkinMAverkinaNAndrasikF. Neurophysiological reactivity before a migraine attack. Neurosci Lett2006; 400: 121–124.
55.
CoppolaGPierelliFSchoenenJ. Is the cerebral cortex hyperexcitable or hyperresponsive in migraine?Cephalalgia2007; 27: 1429–1439.
56.
MullenersWMAuroraSKChronicleE. Self-reported photophobic symptoms in migraineurs and controls are reliable and predict diagnostic category accurately. Headache2000; 41: 31–39.
57.
SandorPSAfraJAmbrosiniA. Prophylactic treatment of migraine with β-blockers and riboflavin: Differential effects on the intensity dependence of auditory evoked cortical potentials. Headache2000; 40: 30–35.
58.
EliasSSalvaiaJShepherdAJ. Symptoms of visual discomfort from automobile LED lights and their correlation with headache in night-time taxi drivers. Light Res Technol2014; 46: 354–363.
59.
DhruvNTCarandiniM. Cascaded effects of spatial adaptation in the early visual system. Neuron2014; 81: 529–535.
60.
LarrsonJHarrisonSJ. Spatial specificity and inheritance of adaptation in human visual cortex. J Neurophysiol2015; 114: 1211–1226.
61.
StockerAASimoncelliEP. Visual motion aftereffects arise from a cascade of two isomorphic adaptation mechanisms. J Vis2009; 9: 9.1–14.–9.1–14..
62.
DhruvNTTailbyCSokolSH. Multiple adaptable mechanisms early in the primate visual pathway. J Neurosci2011; 31: 15016–15025.
63.
ThabetMWilkinsonFWilsonHR. The locus of flicker adaptation in the migraine visual system: A dichoptic study. Cephalalgia2013; 33: 5–19.
64.
FisherRSHardingGErbaG. Photic- and pattern-induced seizures: A review for the Epilepsy Foundation of America Working Group. Epilepsia2005; 46: 1426–1441.
